Новости Сист. Низш. Раст. 51 — Novosti Sist. Nizsh. Rast. 51

Новости сист. низш. раст. — Novosti Sist. Nizsh. Rast. 51: 242–250. 2017

Gemmae in Tetralophozia setiformis (Anastrophyllaceae, Marchantiophyta) and their second record in Eurasia M. V. Dulin Institute of Biology, Komi Science Centre UB RAS, Kommunisticheskaja Str., 28, Syktyvkar, Komi Republic, 167982, Russia; [email protected]

Abstract. Tetralophozia setiformis is a widespread species occurring usually without organs of sexual and asexual reproduction. Gemmae of Tetralophozia setiformis were observed for the second time in Russia and Eurasia in the Northern Urals, Komi Republic. They form compact masses over upper leaves. The compact masses consist largely (70 %) of immature gemmae. Description of gemmae and gemmiparous shoots from the Northern Urals and their comparison with those from the other known localities, namely British Columbia (Canada) and the Murmansk Region (European Russia) were carried out. The gemmiparous plants of T. setiformis from the Northern Urals have approximately the same width as plants without gemmae but they are shorter. The leaves of gemmiparous plants from the Northern Urals are similar to leaves of gemmiparous plants from British Columbia. The leaf shape in upper part of the gemmiparous shoots varies from the typical to ± modiﬁ ed from gemmae production. These leaf shape transitions include reduction of leaf size and lobe number from 4 to 2–3, suppression of development and disappearance of characteristic teeth at the base of sinus. Gemmae size (17 × 22 μm) of plants from the Northern Urals is within variability recorded for plants from the Murmansk Region and British Columbia. Keywords: gemmae, liverworts, Tetralophozia setiformis, British Columbia, Mur- mansk Region, Northern Urals, Komi Republic, Russia.

Выводковые почки у Tetralophozia setiformis (Anastrophyllaceae, Marchantiophyta) и их вторая находка в Евразии М. В. Дулин Институт биологии Коми НЦ УрО РАН, ул. Коммунистическая, д. 28, г. Сыктывкар, 167982, Россия; [email protected]

Резюме. Tetralophozia setifomis — широко распространенный вид, обычно встречающийся в вегетативном состоянии без органов полового и бесполого размножения. Описана вторая находка выводковых почек T. setifomis в России и Евразии и первая на Северном Урале, в Республике Коми. Приведено описа- ние найденных на Северном Урале выводковых почек, побегов, образующих выводковые почки, и их сравнение с данными из двух других известных место- нахождений в Британской Колумбии (Канада) и Мурманской области (Россия). Почкующиеся побеги приблизительно такие же по ширине, но более короткие, с выводковыми почками на верхних листьях в плотных скоплениях, которые об- разованы преимущественно (на 70 %) недозрелыми выводковыми почками. Ли- стья побегов с выводковыми почками с Северного Урала сходны с таковыми из Британской Колумбии. Описаны переходы формы листьев с верхушек почкую-

242 Dulin. Gemmae in Tetralophozia setiformis

щихся побегов от типичных до формирующих выводковые почки, у которых на- блюдалось наряду с уменьшением размеров уменьшение числа лопастей от 4 до 2–3 также уменьшение и исчезновение характерных зубцов в основании выре- зок. Выводковые почки растений с Северного Урала по размерам (17 × 22 мкм) соответствуют ранее выявленному диапазону изменчивости этого признака, но максимальная длина у них меньше. Ключевые слова: выводковые почки, печеночники, Tetralophozia setifomis, Британская Колумбия, Мурманская область, Северный Урал, Республика Коми, Россия. The genus Tetralophozia (R. M. Schust.) Schljakov of the fami- ly Anastrophyllaceae L. Söderstr., De Roo et Hedd. includes four species known from Arctic to tropical latitudes in Asia and Africa (Schus- ter, 2002; Söderström et al., 2010; Söderström et al., 2016). The type of the genus, an arctic-alpine imperfectly circumpolar species T. setiformis (Ehrh.) Schljakov [≡ Chandonanthus setiformis (Ehrh.) Lindb.] is most widespread in the Northern Hemisphere (Konstantinova, 2000; Damsholt, 2002; Schumacker, Váňa, 2005; Konstantinova et al., 2009). Of the four species currently recognized in the genus Tetralophozia (Söderström et al., 2016), gemmae are known only in this species (Schuster, 2002). The plants of T. setiformis are fragile when dry and usually dissemi- nate via fragments. They produce sporophytes and gemmae very rarely. The gemmae were fi rst recognized by Godfrey and Godfrey (1978) from W. B. Schofi eld’s collections obtained from British Columbia. In recent European liverwort identifi cation books (Schljakov, 1980; Damsholt, 2002) there are no description of gemmae. Konstantinova (2002) in her treatment of the genus Tetralophozia for Russia briefl y described and illustrated gemmae of T. setiformis for the fi rst time for Eurasia from the Murmansk Region, Northwest European Russia, however, this reference tends to be overlooked. Then, Damsholt (2013) mentioned that gemmae in T. setiformis are known only from western Canada. In 2016 gemmae of T. setiformis were observed in a collection from the Northern Urals (Komi Republic) that represent the second record of the gemmae in T. setiformis in Eurasia. The purpose of the present paper is to summarize known data on the gemmae of T. setiformis and to provide comparisons from three known distant localities, illustrations and analysis of conditions of their formation. Materials and Methods Habitats and reproduction of Tetralophozia setiformis in the Northern Urals. In the Northern Urals, T. setiformis grows on and between stones at stony fi elds, as well as in small holes and cracks with fi ne

243 Новости сист. низш. раст. — Novosti Sist. Nizsh. Rast. 51: 242–250. 2017 earth in rocky outcrops (remnants and cliffs). It rarely occurs on stones in dwarf-shrub and lichen tundra and on stones along mountain streams. It occurs also on stones in upland light forests, fi r-spruce forests and bushes of Betula nana L. The species occurs in large compact patches or tufts, usually with greenish-, yellowish- or golden-brown to dark brown pig- mentation or as single shoots among other bryophytes such as Tritomaria quinquedentata (Huds.) H. Buch, Sphenolobus minutus (Schreb.) Berggr. Many populations of T. setiformis were observed earlier in the Komi Re- public without organs of sexual or asexual reproduction and reproduce apparently by parts of the shoots and leaf fragments. Plants of T. setiformis are very fragile during dry periods and disseminated by wind, ani- mals, etc. Location of gemmiparous plants of Tetralophozia setiformis in the Northern Urals. Russia: Komi Republic, Northern Urals, Vuktylsky Dis- trict, «Yugyd Va» National Park, the Shchugor River basin, near Halmer- sale Mountain, 3 km SWW of the merger of sources of Halmerya River, 63°48ʹ56.8ʺN; 59°10ʹ48.5ʺE, ca. 715 m alt., lake cirque, steep (45–60°) slope of the cirque, NE exposure, rock outcrops, on ledge in yellowish- brown patches with whitish patches of degraded shoots, 01.07.2016 M. V. Dulin 3ha=1237mvd, SYKO. Gemmiparous shoots were studied using microscopes LOMO MBS 10 and Micmed-2. Shoots were measured after moistening. Prepared leaves and gemmae were selected in separate specimen fi xed by glycerin after microscopy. All observed gemmae (80) and 22 leaves were measured and kept after investigation as separate slides. Maximum values and mean values were calculated on the basis of the obtained measurements. Results Only two gemmiparous shoots of T. setiformis were observed in the specimen cited above. It should be noted that the specimen looks atypical. It contains the plants growing parallel to each other and assembled in compact patches with shoots spread in different directions and interwoven. The latter shoots are shorter and curved. Besides, the main part of plants (up to 50 %) in the specimen has features of degradation expressed in partial or complete yellowing of the plants. It is diffi cult to understand the reasons of such degradation. But, possibly, one of the reasons is being adjacent to the lichen Cladonia coccinifera (L.) Willd. that may affect the plants of T. setiformis by releasing lichen acids characterized by a high antibiotic activity. Such unfavorable condition resulted in degradation of T. setiformis may have initiated gemmae formation in the studied plants. 244 Dulin. Gemmae in Tetralophozia setiformis

Description of gemmiparous plants and gemmae of Tetralophozia setiformis from the Northern Urals (Plate I). The gemmiparous plants of T. setiformis are golden-green to brown. They are smaller in size than non-gemmiparous plants from the same specimen (Table). At the old part of shoots they are 590–760 μm wide, in upper younger narrowed part of the shoots — 320 μm wide and 0.8–1.0 cm long. The leaves of gemmiparous shoots are divided for 0.7–0.9 their length into 3–4 lobes, × 1.0–1.5 as wide as long, 430–700 μm wide × 420–630 μm long; middle leaf lobes are × 1.2–1.9 as long as wide, 310–350 μm long × 160–270 μm wide. At the younger narrowed part of shoots, leaves × 1.0–1.1 as wide as long, 270–320 μm wide × 270–290 long; middle leaf lobes × 1.7–1.8 as long as wide, 170–180 μm long × 100–110 μm wide. Table Variability of morphological features of Tetralophozia setiformis in collections with gemmae Regions Features Murmansk Northern Urals British Columbia Region Nongemmiparous 0.6–1.5 to 6.0 1.6–4.0 shoot length, cm Nongemmiparous (430)540–590(760) (500)700–1100 (680)760–975 shoot width, mm Nongemmiparous (380)430–790(860) to 1000 (770)825–1075 leaf width, μm Nongemmiparous (320)380–540 400–600 (425)450–600 leaf length, μm Nongemmiparous 1.2–1.6 1.7 1.6–2.0 leaf, width/length ratio Gemmiparous shoot 0.8–1.0 «small», no 1.5–2.6 length, cm length mentioned Gemmiparous shoot (320) 590–760 «small», no 400–600(760) width, mm width mentioned Gemmiparous leaf (270–320)430–700 — 350–550 width, μm Gemmiparous leaf (270–290)420–630 — 275–420 length, μm Gemmiparous leaf, 1.0–1.5 — 1.1–1.5 width/length ratio Gemmae size, μm mature: (10)13–18(23) × mature 17–20 × 10–26 × 16–44 (13)18–23(31); 20–30(45) immature: (13)16–18 × (16)18–26(33); juvenile: (13)16–18(21) × (16)18–26(31)

245 Новости сист. низш. раст. — Novosti Sist. Nizsh. Rast. 51: 242–250. 2017

Table continued Regions Features Murmansk Northern Urals British Columbia Region Gemmae shape mature: 3–4(5)-angular, triangular angular, varying fusiform, broadly ovate, from triangular to orbicular; long and spindle- immature: 3–4-angular, shaped rounded-triangular, rounded- quadrate, fusiform, broadly ovate, orbicular, broadly ovoid; juvenile: elliptical, oblong- elliptic, fusiform, broadly ovoid Gemmae color mature: clear deep wine-red mature wine-red mature brilliant, and light wine-red, rare light to bright red deep red to violet- orange-red; red; immature: pale wine-red, immature from pale pale yellowish green, green to golden or pale yellowish red, pale becoming red yellowish-pink, pale pinkish, pale orange-red and colorless; juvenile: pale yellowish green or pale green to colorless 1-celled/2-celled mature 83/17; mainly 2-celled 76/24 gemmae ratio, % immature 81/19; with admixture juvenile 63/37 of 1-celled

The gemmae are abundantly produced in compact masses. They develop in fascicles or singly at the ciliate margins of the youngest leaves and underleaves at the apex of gemmiparous shoots. In total 80 gemmae were investigated and classifi ed into stages of maturity, which were defi ned as follows: mature gemmae clearly wine-red with thickened angles, immature gemmae ± pigmented, ± angulate, with thickened or not angles, juvenile gemmae greenish, ± rounded. Among the studied 80 gemmae, 24 were classifi ed as mature, 40 as immature and 16 as juvenile. Studied mature gemmae were 3–4(5)-angular with admixture of fusiform, broadly ovate and orbicular, (10)13–18(23) × (13)18–23(31) μm, average 18 × 22 μm. Among them predominate 3-angular — 46 %, 4-angular — 29 %, other — 25 %. They are largely 1-celled (83 %) and partly 2-celled (17 %). The immature gemmae are not clearly wine-red. They are mostly pale wine-red (53 %) with admixture of pale yellowish green, pale yellowish red, pale yellowish-pink, pale pinkish, pale orange- red and colorless, with thickened or not angles, (13)16–18 × (16)18– 246 Dulin. Gemmae in Tetralophozia setiformis

26(33) μm, average 17 × 21 μm. Studied immature gemmae largely 1-celled (81 %) and partly 2-celled (19 %), mostly rounded-triangular (55 %) with admixture of 3–4-angular, rounded-quadrate, fusiform, broadly ovate, orbicular, broadly ovoid. Juvenile gemmae pale yellowish green or pale green to colorless and rounded (elliptical, oblong-elliptic, fusiform, broadly ovoid), (13)16–18(21) × (16)18–26(31) μm, averaging 16 × 23 μm. Studied juvenile gemmae largely 1-celled (63 %) and partly 2-celled (37 %). Among all 80 studied gemmae 81% are 1-celled and 19 % are 2-celled. Discussion Most important known data on non-gemmiparous, and gemmiparous shoots and gemmae from all known locations are tabulated (Table). Two earlier recorded localities of gemmiparous plants of T. setiformis are known. 1. Canada, British Columbia, 48 km N of Vancouver, E of Hwy. 99, across from Murrin Prov. Pk. (49°38ʹN; 123°12ʹE), 14.09.1968, W. B. Schofi eld 37872, 37876, 07.06.1974 J. et G. Godfrey 1120; 30.03.1977, B. Tan 1977-2001. All in UBC (Godfrey, Godfrey, 1978). The gemmiparous plants of T. setiformis (recorded as Chandonan- thus setiformis) from southwestern British Columbia are golden-green or, more frequently, golden or reddish-gold. These plants are smaller in size than non-gemmiparous plants from the same site (Godfrey, Godfrey, 1978). The gemmae are formed abundantly in fascicles on the youngest leaves and underleaves at the shoot apex and by pinching off individu- al cells at lobe apices, along margins and at tips of cilia on older leaves and underleaves around and below the shoot apex. It appears that 2-celled gemmae, when present, are formed from the terminal cells or, less frequently, from the second cells in the gemmae fascicles. Mature leaves which have at one time produced gemmae have distinctly eroded margins and often vary considerably from typical leaves on nongemmiparous plants, i. e., leaves are less deeply divided into lobes, lobe number be- comes reduced from 3–4 to 2–3, and there is little indication of teeth between the lobes at their bases (Godfrey, Godfrey, 1978). 2. Russia, Murmansk Region, Khibiny Mountains, Vudyavrchor Moun- tains the territory of Polar-Alpine Botanical Garden-Institute (67°38ʹN; 33°36ʹE), ca. 500 m a. s. l., steep (35–40°) north-east-facing slope, between boulders, with Racomitrium sp., N. A. Konstantinova 1171-12-743 (CRIS (http://kpabg.ru/cris/ KPABG-H 1136)). There are almost no data on the gemmiparous plants from the Mur- mansk Region. It is only known that upper leaves of gemmiparous shoots are dentate to the top (Konstantinova, 2002). Noteworthy, most gem- 247 Новости сист. низш. раст. — Novosti Sist. Nizsh. Rast. 51: 242–250. 2017 mae observed in the plants from the Murmansk Region are described as 2-celled unlike the gemmae from the other locations (Table). Thus the non-gemmiparous plants of T. setiformis from the Northern Urals are smaller than plants from British Columbia and the Murmansk Region (Table). The gemmiparous plants from the Northern Urals are approximately as wide as plants from British Columbia but shorter. The leaves of gemmiparous plants from our collection are similar in size with those from British Columbia. We did not fi nd mature leaves that at the same time have both produced gemmae and distinctly eroded margins and vary considerably from typical leaves on non-gemmiparous plants as reported by Godfrey and Godfrey (1978). However, we have observed on the gemmiparous shoots the transitional forms of leaves from the typical to gemmiparous. In the series of the intermediate forms seve- ral trends were observed: reduction of leaf size and lobe number from 4 to 2–3, suppression of development and disappearance of the typical teeth in the sinus bases of leaves. Gemmae of the plants from the Northern Urals are within the varia- tion limits but have narrower variability in size than gemmae in the plants from the other locations. Their average size is 17 × 22 μm (maximal size 33 μm) while in British Columbia the average gemmae size is 16 × 28 μm (maximal 44 μm), and in the Murmansk Region is 18 × 25 μm (maximal 45 μm). As in the specimens collected in British Columbia, the gemmae in the specimen from the Northern Urals are grouped in dense clusters. Among them immature gemmae dominated and varied widely in color. In our opinion the causes that most likely initiated gemmae formation in T. setiformis in our collection are very harsh habitat conditions and probably lichen infl uence which lead to the degradation of shoots. Find- ing gemmae in such a widespread species in the Ural Mountains, most likely, is not an exception or some anomaly of development. Probably this species generates gemmae during certain periods or in certain years or perhaps infl uenced by other climatic factors. Chances are, with more careful study of patches in the fi eld, the presence of gemmae or atypical shoots will offer a sign of their possible presence, and will add new specimens of T. setiformis with gemmae to the herbarium SYKO. Acknowledgments The author is grateful to A. D. Potemkin for valuable comments and help and to Y. A. Dubrovskij for help in translation of the article. The research was performed under the fi nancial support of the Project № АААА-А16-116021010241-9: «Structural and functional organization of plant communities, diversity of fl ora, lichen- and mycobiota of southern 248 Dulin. Gemmae in Tetralophozia setiformis part of “Yugyd Va” National Park» (2016–2018) and partially supported by the Russian Foundation for Basic Research (project № 15-04-03479-а).

References Damsholt K. 2002. Illustrated fl ora of Nordic liverworts and hornworts. Odense: 840 p. Damsholt K. 2013. The liverworts of Greenland. Lund: 626 p. Godfrey J. D., Godfrey G. A. 1978. Asexual reproduction in Chandonanthus setiformis. Bryologist. 81(2): 326–330. Konstantinova N. A. 2000. Distribution pattern of the North Holarctic hepatics. Arctoa. 9: 29–94. (In Russ. with Engl. abstract). Konstantinova N. A. 2002. The genus Tetralophozia (R. M. Schust.) Schljakov (Lopho- ziaceae, Hepaticae) in Russia. Arctoa. 11: 45–52. (In Russ. with Engl. abstract). Konstantinova N. A., Bakalin V. A., Andrejeva E. N., Bezgodov A. G., Borovichev E. A., Dulin M. V., Mamontov Yu. S. 2009. Checklist of liverworts (Marchan- tiophyta) of Russia. Arctoa. 18: 1–64. (In Russ. and Engl.). Schljakov R. N. 1980. Pechenochniki Severa SSSR. Vyp. 3. Pechenochniki: Lophozia- ceae — Mesoptychiaceae [Hepaticae of the North of the USSR. Iss. 3. Liverworts: Lophoziaceae — Mesoptychiaceae]. Leningrad: 188 p. (In Russ.). Schumacker R, Váňa J. 2005. Identifi cation keys to the liverworts and hornworts of Europe and Macaronesia (Distribution and Status). Poznan: 209 p. Schuster R. M. 2002. Austral Hepaticae. Part II. Nova Hedwigia Beih. 119: 606 p. Söderström L., De Roo R., Hedderson T. 2010. Taxonomic novelties resulting from recent reclassifi cation of the Lophoziaceae/Scapaniaceae clade. Phytotaxa. 3: 47–53. Söderström L., Hagborg A., von Konrat M., Bartholomew-Began Sh., Bell D., Briscoe L., Brown E., Cargill D. Ch., Costa D. P., Crandall-Stotler B. J., Cooper E. D., Dau- phin G., Engel J. J., Feldberg K., Glenny D., Gradstein S. R., He X.-L., Heinrichs J., Hentschel J., Ilkiu-Borges A. L., Katagiri T., Konstantinova N. A., Larraín J., Long D. G., Nebel M., Pócs T., Puche F., Reiner-Drehwald E., Renner M. A. M., Sass- Gyarmati A., Schäfer-Verwimp A., Moragues J. G. S., Stotler R. E., Sukkharak Ph., Thiers B. M., Uribe J., Váňa J., Villarreal J. C., Wigginton M., Zhang L., Zhu R.-L. 2016. World checklist of hornworts and liverworts. PhytoKeys. 59: 1–828.

Литература Damsholt K. 2002. Illustrated ﬂ ora of Nordic liverworts and hornworts. Odense: 840 p. Damsholt K. 2013. The liverworts of Greenland. Lund: 626 p. Godfrey J. D., Godfrey G. A. 1978. Asexual reproduction in Chandonanthus setiformis. Bryologist. 81(2): 326–330. [Konstantinova] Константинова Н. А. 2000. Анализ ареалов печеночников севера Голарктики. Arctoa. 9: 29–94. [Konstantinova] Константинова Н. А. 2002. Род Tetralophozia (R. M. Schust.) Schlja- kov (Lophoziaceae, Hepaticae) в России. Arctoa.11: 45–52. [Konstantinova et al.] Konstantinova N. A., Bakalin V. A., Andrejeva E. N., Bezgodov A. G., Borovichev E. A., Dulin M. V., Mamontov Yu. S. 2009. Список печеночни- ков (Marchantiophyta) России. Arctoa. 18: 1–64.

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[Schljakov] Шляков Р. Н. 1980. Печеночники Севера СССР. Вып. 3. Печеночники: Lophoziaceae — Mesoptychiaceae. Л.: 188 с. Schumacker R, Váňa J. 2005. Identiﬁ cation keys to the liverworts and hornworts of Europe and Macaronesia (Distribution and Status). Poznan: 209 p. Schuster R. M. 2002. Austral Hepaticae. Part II. Nova Hedwigia Beih. 119: 606 p. Söderström L., De Roo R., Hedderson T. 2010. Taxonomic novelties resulting from recent reclassiﬁ cation of the Lophoziaceae/Scapaniaceae clade. Phytotaxa. 3: 47–53. Söderström L., Hagborg A., von Konrat M., Bartholomew-Began Sh., Bell D., Briscoe L., Brown E., Cargill D. Ch., Costa D. P., Crandall-Stotler B. J., Cooper E. D., Dau- phin G., Engel J. J., Feldberg K., Glenny D., Gradstein S. R., He X.-L., Heinrichs J., Hentschel J., Ilkiu-Borges A. L., Katagiri T., Konstantinova N. A., Larraín J., Long D. G., Nebel M., Pócs T., Puche F., Reiner-Drehwald E., Renner M. A. M., Sass- Gyarmati A., Schäfer-Verwimp A., Moragues J. G. S., Stotler R. E., Sukkharak Ph., Thiers B. M., Uribe J., Váňa J., Villarreal J. C., Wigginton M., Zhang L., Zhu R.-L. 2016. World checklist of hornworts and liverworts. PhytoKeys. 59: 1–828. M. V. Dulin (p. 242–250)

Plate I. Tetralophozia setiformis (Ehrh.) Schljakov. 1 — upper part of gemmiparous shoot; 2 — mature gemmae; 3 — immature gemmae; 4 — juvenile gemmae; 5 — gemmiparous leaf with mature gemmae; 6 — upper gemmiparous leaf from gemmiparous shoot; 7 — fascicles of gemmae; 8 — gemmiparous shoots; 9 — nongemmiparous shoot; 10 — underleaf from gemmiparous shoot; 11, 12 — leaves from middle part of gemmiparous shoot; 13 — upper leaf from gemmiparous shoot; 14 — typical leaf from nongemmiparous shoot; 15 — typical underleaf from nongemmiparous shoot. Scale bars: 1, 10–15 — 100 μm; 2–7 — 25 μm; 8, 9 — 2 mm. All from 01.07.2016 M. V. Dulin 3ha=1237mvd, SYKO.